Considered one of the sport's greatest scrum halves, Howley began his domestic career at Bridgend, later moving to Cardiff. He reverted back to Bridgend and once more moved to Cardiff before leaving for London Wasps in 2002 on a three year contract. However, a serious wrist injury forced him to cut his career short just months after his last minute try against Toulouse saw him lifting the Heineken Cup with Wasps in 2004 Final at Twickenham.

Howley gained fifty-nine caps for Wales and captained his country on 22 occasions between 1998 and 1999. He was the Welsh Player of the Year in 1996 and 1997 and was a member of British and Irish Lions tours, in 1997 to South Africa and 2001 to Australia.

Howley played in the 1999 Rugby World Cup, captaining his country in the process until he left the field injured against Australia in the dying minutes of the quarter-final. He was selected for the 1997 British & Irish Lions tour to South Africa but suffered a shoulder injury and couldn't play in the test matches. He played in the first two Tests of the 2001 British & Irish Lions tour to Australia before a broken rib ruled him out of the series decider against the Wallabies; a tour in which he was one of the tour captains.

Howley's last game for Wales was against Scotland at Murrayfield in April 2002, he then turned his attention to club rugby for the remainder of his playing career. After a domestic career divided between Bridgend and Cardiff, Howley joined Wasps in 2002 and would later score a last-minute try to seal a 27-20 victory over Toulouse in the 2004 Heineken Cup Final.

Following his retirement from playing Howley coached the Cardiff Blues before moving on to join the Wales coaching staff under Warren Gatland in 2008. He began his work with the national side as attack coach and later linked up with the British & Irish Lions for their tour of South Africa in 2009.

After helping Wales to the semi-finals of the 2011 Rugby World Cup as assistant coach, Howley put pen to paper on a new deal with the Welsh Rugby Union that will see him continue to work alongside Gatland until at least 2016. Howley helped guide Wales to their third Grand Slam in eight years with a clean sweep in the 2012 Championship and when Gatland was later sidelined with two broken ankles following a domestic accident, Howley was made caretaker coach for that summer's tour of Australia.

Under Howley's guidance Wales lost all three tests - albeit all by narrow margins - and suffered humbling defeats to Samoa and Argentina during the autumn internationals. However, despite struggling as interim head coach for the national team, Howley was named as one of Warren Gatland's three assistant coaches for the British & Irish Lions' tour of Australia.